Abstract
How soil microbial communities respond to precipitation seasonality change remains poorly understood, particularly for warm-humid forest ecosystems experiencing clear dry-wet cycles. We conducted a field precipitation manipulation experiment in a subtropical forest to explore the impacts of reducing dry-season rainfall but increasing wet-season rainfall on soil microbial community composition and enzyme activities. A 67% reduction of throughfall during the dry season decreased soil water content (SWC) by 17–24% (P < 0.05), while the addition of water during the wet season had limited impacts on SWC. The seasonal precipitation redistribution had no significant effect on the microbial biomass and enzyme activities, as well as on the community composition measured with phospholipid fatty acids (PLFAs). However, the amplicon sequencing revealed differentiated impacts on bacterial and fungal communities. The dry-season throughfall reduction increased the relative abundance of rare bacterial phyla (Gemmatimonadetes, Armatimonadetes, and Baoacteriodetes) that together accounted for only 1.5% of the total bacterial abundance by 15.8, 40, and 24% (P < 0.05), respectively. This treatment also altered the relative abundance of the two dominant fungal phyla (Basidiomycota and Ascomycota) that together accounted for 72.4% of the total fungal abundance. It increased the relative abundance of Basidiomycota by 27.4% while reduced that of Ascomycota by 32.6% (P < 0.05). Our results indicate that changes in precipitation seasonality can affect soil microbial community composition at lower taxon levels. The lack of community-level responses may be ascribed to the compositional adjustment among taxonomic groups and the confounding effects of other soil physicochemical variables such as temperature and substrate availability.
Similar content being viewed by others
References
Allison SD, Martiny JB (2008) Resistance, resilience, and redundancy in microbial communities. Proc Nati Acad Sci USA 105:11512–11519
Atlas RM, Bartha R (1998) Microbial ecology: fundamentals and applications, 4th edn. Benjamin-Cummings, California
Baldrian P, Valaskova V (2008) Degradation of cellulose by basidiomycetous fungi. FEMS Microbiol Rev 32:501–521
Barnard RL, Osborne CA, Firestone MK (2013) Responses of soil bacterial and fungal communities to extreme desiccation and rewetting. ISME J 7:2229–2241
Beier C, Beierkuhnlein C, Wohlgemuth T, Peñuelas J, Emmett B, Korner C, de Boeck H, Christensen JH, Leuzinger S, Janssens IA, Hansen K (2012) Precipitation manipulation experiments—challenges and recommendations for the future. Ecol Lett 15:899–911
Bell CW, Tissue DT, Loik ME, Wallenstein MD, Acosta-Martinez V, Erickson RA, Zak JC (2014) Soil microbial and nutrient responses to 7 years of seasonally altered precipitation in a Chihuahuan Desert grassland. Glob Chang Biol 20:1657–1673
Bouskill NJ, Lim HC, Borglin S, Salve R, Wood TE, Silver WL, Brodie EL (2013) Pre-exposure to drought increases the resistance of tropical forest soil bacterial communities to extended drought. ISME J 7:384–394
Brando PM, Nepstad DC, Davidson EA, Trumbore SE, Ray D, Camargo P (2008) Drought effects on litterfall, wood production and belowground carbon cycling in an Amazon forest: results of a throughfall reduction experiment. Philos Trans R Soc B-Biol Sci 363:1839–1848
Brockett BFT, Prescott CE, Grayston SJ (2012) Soil moisture is the major factor influencing microbial community structure and enzyme activities across seven biogeoclimatic zones in western Canada. Soil Biol Biochem 44:9–20
Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842
Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, Weintraub MN, Zoppini A (2012) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624
Carney KM, Matson PA (2005) Plant communities, soil microorganisms, and soil carbon cycling: does altering the world belowground matter to ecosystem functioning? Ecosystems 8:928–940
Castro HF, Classen AT, Austin EE, Norby RJ, Schadt CW (2010) Soil microbial community responses to multiple experimental climate change drivers. Appl Environ Microbiol 76:999–1007
Cavaleri MA, Reed SC, Smith WK, Wood TE (2015) Urgent need for warming experiments in tropical forests. Glob Chang Biol 21:2111–2121
Ciardi C, Ceccanti B, Nannipieri P, Casella S, Toffanin A (1993) Effect of various treatments on contents of adenine nucleotides and RNA of Mediterranean soils. Soil Biol Biochem 25:739–746
Costa ACL, Galbraith D, Almeida S, Portela BTT, Costa M, Joao ASJ, Braga AP, Goncalves PHL, Oliveira AAR, Fisher R, Phillips OL, Metcalfe DB, Levy P, Meir P (2010) Effect of 7 yr of experimental drought on vegetation dynamics and biomass storage of an eastern Amazonian rainforest. New Phytol 187:579–591
DeBruyn JM, Nixon LT, Fawaz MN, Johnson AM, Radosevich M (2011) Global biogeography and quantitative seasonal dynamics of Gemmatimonadetes in soil. Appl Environ Microbiol 77:6295–6300
Delgado-Baquerizo M, Maestre FT, Reich PB, Jeffries TC, Gaitan JJ, Encinar D, Berdugo M, Campbell CD, Singh BK (2016) Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat Commun. doi:10.1038/ncomms10541
Drenovsky RE, Vo D, Graham KJ, Scow KM (2004) Soil water content and organic carbon availability are major determinants of soil microbial community composition. Microb Ecol 48:424–430
Drenovsky RE, Steenwerth KL, Jackson LE, Scow KM (2010) Land use and climatic factors structure regional patterns in soil microbial communities. Glob Ecol Biogeogr 19:27–39
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998
Fang X, Zhou G, Li Y, Liu S, Chu G, Xu Z, Liu J (2016) Warming effects on biomass and composition of microbial communities and enzyme activities within soil aggregates in subtropical forest. Biol Fertil Soils 52:353–365
Fang Y, Gundersen P, Mo J, Zhu W (2008) Input and output of dissolved organic and inorganic nitrogen in subtropical forests of South China under high air pollution. Biogeosciences 5:339–352
Fazi S, Amalfitano S, Pernthaler J, Puddu A (2005) Bacterial communities associated with benthic organic matter in headwater stream microhabitats. Environ Microbiol 7:1633–1640
Fierer N, Leff JW, Adams BJ, Nielsen UN, Bates ST, Lauber CL, Owens S, Gilbert JA, Wall DH, Caporaso JG (2012) Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proc Nati Acad Sci USA 109:21390–21395
Frostegård Å, Bååth E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22:59–65
German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD (2011) Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43:1387–1397
Gimbel KF, Felsmann K, Baudis M, Puhlmann H, Gessler A, Bruelheide H, Kayler Z, Ellerbrock RH, Ulrich A, Welk E, Weiler M (2015) Drought in forest understory ecosystems—a novel rainfall reduction experiment. Biogeosciences 12:961–975
Goodfellow M, Williams ST (1983) Ecology of Actinomycetes. Annu Rev Microbiol 37:189–216
Griffiths BS, Bonkowski M, Roy J, Ritz K (2001) Functional stability, substrate utilisation and biological indicators of soils following environmental impacts. Appl Soil Ecol 16:49–61
Gutknecht JLM, Henry HAL, Balser TC (2010) Inter-annual variation in soil extra-cellular enzyme activity in response to simulated global change and fire disturbance. Pedobiologia 53:283–293
Harris RF (1981) Effect of water potential on microbial growth and activity. In: Parr JF, Gardner WR, Elliott LF (Eds) Water potential relations in soil microbiology. Soil Science Society of America, Madison, WI, pp. 23–95
Henry HAL (2012) Reprint of “soil extracellular enzyme dynamics in a changing climate”. Soil Biol Biochem 56:53–59
Henry HAL, Juarez JD, Field CB, Vitousek PM (2005) Interactive effects of elevated CO2, N deposition and climate change on extracellular enzyme activity and soil density fractionation in a California annual grassland. Glob Change Biol 11:1808–1815
Högberg MN, Yarwood SA, Myrold DD (2014) Fungal but not bacterial soil communities recover after termination of decadal nitrogen additions to boreal forest. Soil Biol Biochem 72:35–43
Huang G, Li Y, Su Y (2015) Effects of increasing precipitation on soil microbial community composition and soil respiration in a temperate desert, Northwestern China. Soil Biol Biochem 83:52–56
Hueso S, García C, Hernández T (2012) Severe drought conditions modify the microbial community structure, size and activity in amended and unamended soils. Soil Biol Biochem 50:167–173
IPCC (2013) Climate change 2013: the physical science basis. Working Group I Contribution to the IPCC Fifth Assessment Report
Jackson RB, Fierer N, Schimel JP (2007) New directions in microbial ecology. Ecology 88:1343–1344
Joergensen RG, Wu J, Brookes PC (2011) Measuring soil microbial biomass using an automated procedure. Soil Biol Biochem 43:873–876
Kieft TL, Soroker E, Firestone MK (1987) Microbial biomass response to a rapid increase in water potential when dry soil is wetted. Soil Biol Biochem 19:119–126
Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277
Kreyling J, Beierkuhnlein C, Elmer M, Pritsch K, Radovski M, Schloter M, Wöllecke J, Jentsch A (2008) Soil biotic processes remain remarkably stable after 100-year extreme weather events in experimental grassland and heath. Plant Soil 308:175–188
Landesman WJ, Dighton J (2010) Response of soil microbial communities and the production of plant-available nitrogen to a two-year rainfall manipulation in the New Jersey Pinelands. Soil Biol Biochem 42:1751–1758
Leps J, Smilauer P (2003) Multivariate analysis of ecological data using CANOCO. Cambridge University Press, Cambridge, Cambridge
Liu L, Wang X, Lajeunesse MJ, Miao G, Piao S, Wan S, Wu Y, Wang Z, Yang S, Li P, Deng M (2016a) A cross-biome synthesis of soil respiration and its determinants under simulated precipitation changes. Glob Change Biol 22:1394–1405
Liu W, Allison SD, Xia J, Liu L, Wan S (2016b) Precipitation regime drives warming responses of microbial biomass and activity in temperate steppe soils. Biol Fertil Soils 52:469–477
Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R (2011) UniFrac: an effective distance metric for microbial community comparison. ISME J 5:69–172
Ma L, Guo C, Lu X, Yuan S, Wang R (2015) Soil moisture and land use are major determinants of soil microbial community composition and biomass at a regional scale in northeastern China. Biogeosciences 12:2585–2596
Maestre FT, Delgado-Baquerizo M, Jeffries TC, Eldridge DJ, Ochoa V, Gozalo B, Quero JL, Garcia-Gomez M, Gallardo A, Ulrich W, Bowker MA, Arredondo T, Barraza-Zepeda C, Bran D, Florentino A, Gaitan J, Gutierrez JR, Huber-Sannwald E, Jankju M, Mau RL, Miriti M, Naseri K, Ospina A, Stavi I, Wang DL, Woods NN, Yuan X, Zaady E, Singh BK (2015) Increasing aridity reduces soil microbial diversity and abundance in global drylands. Proc Nati Acad Sci USA 112:15684–15689
Manzoni S, Schimel JP, Porporato A (2012) Responses of soil microbial communities to water stress: results from a meta-analysis. Ecology 93:930–938
Marschner P (2007) Soil microbial community structure and function assessed by FAME, PLFA and DGGE—advantages and limitations. In: Varma A, Oelmüller R (eds) Advanced techniques in soil microbiology. Springer, Berlin, pp. 181–200
Matulich KL, Weihe C, Allison SD, Amend AS, Berlemont R, Goulden ML, Kimball S, Martiny AC, Martiny JB (2015) Temporal variation overshadows the response of leaf litter microbial communities to simulated global change. ISME J 9:2477–2489
Nannipieri P, Giagnoni L, Renella G, Puglisi E, Ceccanti B, Masciandaro G, Fornasier F, Moscatelli MC, Marinari S (2012) Soil enzymology: classical and molecular approaches. Biol Fertil Soils 48:743–762
Nemergut DR, Townsend AR, Sattin SR, Freeman KR, Fierer N, Neff JC, Bowman WD, Schadt CW, Weintraub MN, Schmidt SK (2008) The effects of chronic nitrogen fertilization on alpine tundra soil microbial communities: implications for carbon and nitrogen cycling. Environ Microbiol 10:3093–3105
Nepstad DC, Moutinho P, Dias-Filho MB, Davidson E, Cardinot G, Markewitz D, Figueiredo R, Vianna N, Chambers J, Ray D, Guerreiros JB, Lefebvre P, Sternberg L, Moreira M, Barros L, Ishida FY, Tohlver I, Belk E, Kalif K, Schwalbe K (2002) The effects of partial throughfall exclusion on canopy processes, aboveground production, and biogeochemistry of an Amazon forest. J Geophys Res. doi:10.1029/2001JD000360
Pathan SI, Ceccherini MT, Hansen MA, Giagnoni L, Ascher J, Arenella M, Sørensen SJ, Pietramellara G, Nannipieri P, Renella G (2015) Maize lines with different nitrogen use efficiency select bacterial communities with different β-glucosidase-encoding genes and glucosidase activity in the rhizosphere. Biol Fertil Soils 51:995–1004
Rees GN, Baldwin DS, Watson GO, Perryman S, Nielsen DL (2004) Ordination and significance testing of microbial community composition derived from terminal restriction fragment length polymorphisms: application of multivariate statistics. Anton Leeuw Int J G 86:339–347
Reichmann LG, Sala OE, Peters Debra PC (2013) Water controls on nitrogen transformations and stocks in an arid ecosystem. Ecosphere. doi:10.1890/ES12-00263.1
Rocca JD, Hall EK, Lennon JT, Evans SE, Waldrop MP, Cotner JB, Nemergut DR, Graham EB, Wallenstein MD (2015) Relationships between protein-encoding gene abundance and corresponding process are commonly assumed yet rarely observed. ISME J 9:1693–1699
Sardans J, Peñuelas J (2005) Drought decreases soil enzyme activity in a Mediterranean Quercusilex L. forest. Soil Biol Biochem 37:455–461
Saiya-Cork KR, Sinsabaugha RL, Zak DR (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315
Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol. doi:10.1186/gb-2011-12-6-r60
Shen W, Jenerette GD, Hui D, Scott RL (2016) Precipitation legacy effects on dryland ecosystem carbon fluxes: direction, magnitude and biogeochemical carryovers. Biogeosciences 13:425–439
Shi A, Marschner P (2015) The number of moist days determines respiration in drying and rewetting cycles. Biol Ferti Soils 51:33–41
Singh BK, Bardgett RD, Smith P, Reay DS (2010) Microorganisms and climate change: terrestrial feedbacks and mitigation options. Nat Rev Microbiol 8:779–790
Sinsabaugh RL, Gallo ME, Lauber C, Waldrop MP, Zak DR (2005) Extracellular enzyme activities and soil organic matter dynamics for northern hardwood forests receiving simulated nitrogen deposition. Biogeochemistry 75:201–215
Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, Stursova M, Takacs-Vesbach C, Waldrop MP, Wallenstein MD, Zak DR, Zeglin LH (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264
Sinsabaugh RL (2010) Phenol oxidase, peroxidise and organic matter dynamics of soil. Soil Biol Biochem 42:391–404
Sinsabaugh RL, Follstad Shah JJ (2012) Ecoenzymatic stoichiometry and ecological theory. Annu Rev Ecol Evol Syst 43:313–343
Soil Survey Staff (2010) Keys to soil taxonomy. Unite States Department of Agriculture-Natural Resources Conservation Service, Washington, DC
Sorensen PO, Germino MJ, Feris KP (2013) Microbial community responses to 17 years of altered precipitation are seasonally dependent and coupled to co-varying effects of water content on vegetation and soil C. Soil Biol Biochem 64:155–163
Toberman H, Freeman C, Evans C, Fenner N, Artz RR (2008) Summer drought decreases soil fungal diversity and associated phenol oxidase activity in upland Calluna heathland soil. FEMS Microbiol Ecol 66:426–436
Tuttle S, Salvucci G (2016) Empirical evidence of contrasting soil moisture-precipitation feedbacks across the United States. Science 352:825–828
Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707
Waldrop MP, Firestone MK (2006) Response of microbial community composition and function to soil climate change. Microb Ecol 52:716–724
Waring BG, Hawkes CV (2015) Short-term precipitation exclusion alters microbial responses to soil moisture in a wet tropical forest. Microb Ecol 69:843–854
Williams MA, Rice CW (2007) Seven years of enhanced water availability influences the physiological, structural, and functional attributes of a soil microbial community. Appl Soil Ecol 35:535–545
White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA et al (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp. 315–322
Yavitt JB, Wright SJ, Wieder RK (2004) Seasonal drought and dry-season irrigation influence leaf-litter nutrients and soil enzymes in a moist, lowland forest in Panama. Austral Ecol 29:177–188
Yu G, Chen Z, Piao S, Peng C, Ciais P, Wang Q, Li X, Zhu X (2014) High carbon dioxide uptake by subtropical forest ecosystems in the East Asian monsoon region. Proc Nati Acad Sci USA 111:4910–4915
Zhou G, Wei X, Wu Y, Liu S, Huang Y, Yan J, Zhang D, Zhang Q, Liu J, Meng Z, Wang C, Chu G, Liu S, Tang X, Liu X (2011) Quantifying the hydrological responses to climate change in an intact forested small watershed in Southern China. Glob Change Biol 17:3736–3746
Zhou W, Hui D, Shen W (2014) Effects of soil moisture on the temperature sensitivity of soil heterotrophic respiration: a laboratory incubation study. PLoS One. doi:10.1371/journal.pone.0092531
Acknowledgements
We gratefully acknowledge Mr. Zhipeng Chen, Mozheng Li, and Shengxing Fu for their helps on field works; Mrs. Chunqing Long, Xiaoli Wang, and Mr. Quan Chen for their helps on laboratory analysis; and Miss Susan Nuske for language polishing. Financial supports came from the Natural Science Foundation of China (31130011, 31425005, and 31290222), the Guangdong Science and Technology Program (2016A030303044), and the International Partnership Program for Creative Research Teams of the Chinese Academy of Sciences.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Qian Zhao and Shuguang Jian contributed equally to this work.
Electronic supplementary material
ESM 1
(DOCX 818 kb)
Rights and permissions
About this article
Cite this article
Zhao, Q., Jian, S., Nunan, N. et al. Altered precipitation seasonality impacts the dominant fungal but rare bacterial taxa in subtropical forest soils. Biol Fertil Soils 53, 231–245 (2017). https://doi.org/10.1007/s00374-016-1171-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-016-1171-z